Enhanced Transformation of Tetrabromobisphenol A by Nitrifiers in

Mar 10, 2015 - Yujie Men , Ping Han , Damian E. Helbling , Nico Jehmlich , Craig Herbold , Rebekka Gulde , Annalisa Onnis-Hayden , April Z. Gu , David...
9 downloads 14 Views 760KB Size
Article pubs.acs.org/est

Enhanced Transformation of Tetrabromobisphenol A by Nitrifiers in Nitrifying Activated Sludge Fangjie Li,† Bingqi Jiang,‡ Peter Nastold,§ Boris Alexander Kolvenbach,§ Jianqiu Chen,∥ Lianhong Wang,† Hongyan Guo,† Philippe François-Xavier Corvini,†,§ and Rong Ji*,†,⊥ †

State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, 163 Xianlin Avenue, 210023 Nanjing, China ‡ Fujian Provincial Academy of Environmental Science, No. 10, Huan Bei San Cun, Fuzhou 350013, China § Institute for Ecopreneurship, School of Life Sciences, University of Applied Sciences and Arts Northwestern Switzerland, Gründenstrasse 40, Muttenz CH-4132, Switzerland ∥ Department of Environmental Science, China Pharmaceutical University, Tongjia Alley 24, 210009 Nanjing, China ⊥ Institute for Marine Science & Institute for Climate and Global Change Research, Nanjing University, 22 Hankou Road, 210093 Nanjing, China S Supporting Information *

ABSTRACT: The fate of the most commonly used brominated flame retardant, tetrabromobisphenol A (TBBPA), in wastewater treatment plants is obscure. Using a 14C-tracer, we studied TBBPA transformation in nitrifying activated sludge (NAS). During the 31-day incubation, TBBPA transformation (half-life 10.3 days) was accompanied by mineralization (17% of initial TBBPA). Twelve metabolites, including those with single benzene ring, O-methyl TBBPA ether, and nitro compounds, were identified. When allylthiourea was added to the sludge to completely inhibit nitrification, TBBPA transformation was significantly reduced (half-life 28.9 days), formation of the polar and single-ring metabolites stopped, but O-methylation was not significantly affected. Abiotic experiments confirmed the generation of mono- and dinitro-brominated forms of bisphenol A in NAS by the abiotic nitration of TBBPA by nitrite, a product of ammonia-oxidizing microorganisms (AOMs). Three biotic (type II ipso-substitution, oxidative skeletal cleavage, and Omethylation) and one abiotic (nitro-debromination) pathways were proposed for TBBPA transformation in NAS. Apart from Omethylation, AOMs were involved in three other pathways. Our results are the first to provide information about the complex metabolism of TBBPA in NAS, and they are consistent with a determining role for nitrifiers in TBBPA degradation by initiating its cleavage into single-ring metabolites that are substrates for the growth of heterotrophic bacteria. thermal decomposition, or biotransformation.11−13 Among these, microbial transformation is a key process determining the fate of pollutants in environmental systems. Most studies assessing this route have reported reductive debromination of TBBPA under anoxic conditions in soils, sediments, and sewage sludges. The products of this reaction are lower brominated intermediates11−16 and, ultimately, bisphenol A (BPA).12,17−20 Liu et al.12 showed that the debromination of TBBPA in anoxic soil was accompanied by the formation of large amounts of nonextractable (bound) residues that release brominated BPAs into soil exposed to the air. By contrast, little is known about the transformation of TBBPA under oxic conditions. In aquatic

1. INTRODUCTION Tetrabromobisphenol A [4,4′-isopropylidenebis(2,6-dibromophenol), TBBPA] is the most commonly used brominated flame retardant (BFR) worldwide.1 Its primary applications are in printed circuit boards as a reactive flame retardant and in plastic polymers as an additive. However, because of its extensive use, TBBPA has become a ubiquitous environmental contaminant, frequently detected in air, dust, water, sewage sludge, sediment, soil, and human and animal tissues.1−7 Evidence of the adverse effects of TBBPA release into the environment is substantial. For example, TBBPA was shown to exhibit significant thyroid- and estrogen-hormone activity3 as well as hepatotoxicity, immunotoxicity, nephrotoxicity, and neurotoxicity.3,8−10 Despite the widespread use of TBBPA, only a limited number of studies have examined its transformation in the environment, whether by photo-oxidation, chemical oxidation, © 2015 American Chemical Society

Received: Revised: Accepted: Published: 4283

December 5, 2014 February 24, 2015 March 9, 2015 March 10, 2015 DOI: 10.1021/es5059007 Environ. Sci. Technol. 2015, 49, 4283−4292

Article

Environmental Science & Technology

2. MATERIALS AND METHODS 2.1. 14C-Labeled TBBPA. Uniformly 14C-ring-labeled TBBPA (14C-TBBPA) was synthesized from uniformly 14Cring-labeled phenol (14C-phenol) in two steps: In the first, 14Cphenol was converted to 14C-ring-labeled BPA (14C-BPA), which in the second was brominated by N-bromosuccinimide to 14C-TBBPA.13 The synthesized 14C-TBBPA had a specific radioactivity of 1.48 × 109 Bq/mmol, a chemical purity of 97%, and a radiochemical purity of 99%. 2.2. Preparation of NAS. Activated sludge was collected from a nitrification tank of a municipal WWTP in Jiangxinzhou, Nanjing, China. The WWTP had a capacity of 600000 population equivalents and a daily flow rate of 260000 m3. The ammonium level in the influent is normally about 20−30 mg N/L. The sludge was allowed to settle and then washed three times with 0.1 M phosphate buffer (pH 7.5) to remove the NH4+, NO2−, and NO3− contained in the sludge, as described by Ren et al.47 The precipitate (biomass) was then resuspended in mineral salts medium (MSM) (pH 7.5), composed of (per L) 0.20 g of MgSO4·7H2O, 0.08 g of CaCl2·2H2O, 0.20 g of KH2PO4·H2O, and 6 mg of Fe−EDTA. The mixed liquor suspended solids (MLSS) was amended with an initial N concentration (in the form of NH4Cl) of 10 mg/L to ensure the growth of AOMs. The mixture was aerated for 1 day at room temperature (25 °C) to reduce the content of dissolved organic matter. This NAS, with an initial ammoniaoxidizing activity of about 50 mg NH4+-N/g SS/h, was used for the biotransformation experiments. 2.3. Transformation of TBBPA in NAS. Aliquots of a methanolic solution of 14C-TBBPA (each 8.33 kBq) were added to 50-mL Erlenmeyer flasks, and the solvent was evaporated under a gentle stream of nitrogen gas. The flasks were then filled with 15 mL of NAS (1500 mg MLSS/L) in MSM (pH 7.5) containing 50 mg of NH4+-N (in the form of NH4Cl)/L. In each flask, the final concentration of TBBPA was 1 mg/L, which was too low to inhibit ammonia-oxidizing activity (Supporting Information, Figure S1). The pH of the mixture was kept at 7.5−8.0 by titration with Na2CO3 (40 g/L) during the incubation. The flasks were then closed with polytetrafluoroethylene-wrapped rubber stoppers. 14CO2 released from the sludge was trapped by 1.0 mL of NaOH (2 M) contained in a 6 mL vial suspended from the bottom of the stopper. All flasks were incubated at 30 °C in the dark with rotary shaking (150 rpm). The flasks were opened several times daily to allow the exchange of headspace gas with atmospheric air, thus ensuring an oxic state in the suspension. During the incubation, the NH4+ concentration in the flasks was monitored daily to track ammonia-oxidizing activity. Ammonia depletion was compensated by the addition of concentrated NH4Cl (10 g N/L) to keep the concentration of NH4+-N at approximately 50 mg/L. The same setup but with the addition of the nitrification inhibitor allylthiourea (ATU, 50 mg/L) to the MSM was used to evaluate TBBPA biotransformation under suppressed ammonia-oxidizing activity. The abiotic transformation of TBBPA in NAS was evaluated using sterilized sludge (autoclaved at 120 °C for 2 × 30 min within two consecutive days). At each sampling time, three flasks from each treatment were removed to analyze the radioactivity in the NaOH trap and the amounts of 14C-TBBPA, its metabolites, and the bound residues (see below). 2.4. Fractionation of Radioactivity in Sludge. The sludge mixture in the flasks was acidified with HCl (1 M) to pH

systems, TBBPA can be biotransformed by algae via sulfation, glucosylation, O-methylation, and debromination.21 Aerobic transformation of TBBPA in the environment reportedly proceeds via O-methylation, yielding mono- and dimethyl ethers of TBBPA (MeO-TBBPA and diMeO-TBBPA, respectively).13,22−24 The O-methylation metabolites are strongly lipophilic and are therefore highly likely to bioaccumulate in the food chain.11 In addition to Omethylation, oxidative skeletal rearrangement, ipso-substitution, and debromination were recently reported as primary pathways of TBBPA transformation in an oxic soil slurry.13 For many organic pollutants, sewage sludge of wastewater treatment plants (WWTPs) serves as a relevant temporary storage compartment or terminal sink. Consequently, the role of WWTPs in the release of pollutants is an issue of growing concern. TBBPA has been detected in effluent samples25 and sewage sludge samples of municipal WWTPs in various countries.25−29 TBBPA was detected at concentrations up to 472 and 732 mg/kg dry weight in sewage sludge samples from Spain29 and China,30 respectively. TBBPA was also the most frequently identified bisphenol analogue in 52 municipal sewage sludge samples collected from 30 cities in China.31 In addition, diMeO-TBBPA has been detected in sludge of WWTPs.32 Because TBBPA has a very low solubility (0.17− 4.16 mg L−1 at 25 °C) and a high octanol/water partition coefficient (log KOW = 4.5−6.5) at neutral pH,33 it sorbs onto sludge flocs, leading to its release in soils in regions where the sludge is applied as fertilizer on agricultural lands. Contradictory results have been reported for the degradation of TBBPA in activated sludges. While according to Brenner et al.15 TBBPA was not degraded in activated sludge under either oxic or anoxic conditions for 4−6 months, the rapid degradation of TBBPA, with a half-life of 0.59 days, was reported in an anoxic sewage sludge.20 Moreover, aerobic bacteria capable of utilizing TBBPA have been isolated from activated sludges.34,35 Nonetheless, our understanding of the degradation of TBBPA in activated sludge is still limited. WWTPs operated for nitrogen removal may enhance the biotransformation of micropollutants.36 The first step of nitrification (i.e., the oxidation of ammonia) is carried out by ammonia-oxidizing microorganisms (AOMs), which oxidize ammonia to hydroxylamine via the enzyme ammonia monooxygenase. Hydroxylamine is further transformed to nitrite by hydroxylamine oxidoreductase. Ammonia monooxygenase also oxidizes a wide range of aliphatic, aromatic, and halogenated hydrocarbons.37 Previous studies have demonstrated the transformation of natural and synthetic estrogens by nitrifying activated sludge (NAS).38−40 Although transformation has been attributed to cometabolism involving AOMs,39,40 the results of recent studies point to abiotic nitration between nitrite and micropollutants in the transformation of the latter during nitrification.41−45 The removal of TBBPA in a nitrifying membrane-activated bioreactor provided further evidence of a key role for nitrification,46 but whether the nitrifying activity within activated sludges is involved in TBBPA degradation is unknown. In this study, a 14C-tracer was used to obtain detailed information about the degradation of TBBPA in NAS, including the fate and metabolism of TBBPA, and to determine the role played by nitrifying activity in the degradation of TBBPA in this activated sludge. 4284

DOI: 10.1021/es5059007 Environ. Sci. Technol. 2015, 49, 4283−4292

Article

Environmental Science & Technology

scintillation cocktail. There was no significant difference between direct counting and the combustion method for the measurement of radioactivity in the sludge. Data Analysis. Data on TBBPA degradation were fitted to the first-order kinetics Ct = C0e−kt, where C0 is the initial concentration, Ct is the concentration at time t, and k is the degradation rate constant. The regression was carried out using SigmaPlot 12.0. The half-life (t1/2) was calculated using the equation t1/2 = ln 2/k. Significance was analyzed using Student’s t-test; a statistical probability of P < 0.05 was considered significant.

2 and immediately extracted with ethyl acetate four times (each 20 mL) by vigorous vortexing (4 min) and centrifugation (3500g, 10 min). The supernatants were combined and dried by passage through a column of anhydrous sodium sulfate. The radioactivity in the extracts was measured by a liquid scintillation counter (LSC, see below) and defined as extractable radioactivity. The extraction recovery of 14CTBBPA from the sludge was 97 ± 2%. The organic extracts were evaporated to dryness using a rotary evaporator at 40 °C, resuspended in 1 mL of methanol, and analyzed by highperformance liquid chromatography (HPLC) coupled to a radio flow detector with liquid scintillation counting (HPLC−14C-LSC, see below). Acidification of the sludge mixture followed by immediate extraction using ethyl acetate did not generate nitro compounds (see the Supporting Information). The radioactivity remaining in the sludge solid after exhaustive extraction with organic solvent was defined as the radioactivity in bound residues and was measured by LSC (see below). 2.5. Abiotic Transformation of TBBPA by Nitrite. Abiotic transformation of TBBPA was assayed in 10 mM phosphate buffer (15 mL) containing 1 mg of 14C-TBBPA (1.67 kBq)/L and 20 or 200 mg of NO2−-N (in the form of NaNO2)/L at pH 6.0 and 7.5 in 50-mL flasks. The flasks were incubated at 30 °C in the dark with rotary shaking (150 rpm). On days 2, 5, and 30, two flasks were removed and the concentrations of 14C-TBBPA and its reaction products were analyzed. Briefly, the aqueous solution in each flask was acidified (pH 2) and then extracted twice with 10 mL of ethyl acetate. The organic extracts were combined, dried by passage through a column of anhydrous sodium sulfate, evaporated to dryness, and resuspended in 1 mL of methanol. These samples were analyzed by HPLC−14C-LSC and liquid chromatography coupled to a mass spectrometer (LC−MS, see below). 2.6. Analyses. HPLC−14C-LSC. HPLC was performed on a Nucleosil C18 column at 40 °C with an Agilent HPLC series 1100 system (Agilent Technologies, Germany) coupled to a diode-array detector and an online radio-flow detector (RAMONA Star; Raytest, Straubenhardt, Germany; for details, see the Supporting Information). Purification of the Transformation Products (TPs). Aliquots (200 μL) of the methanolic extract of NAS containing high concentrations of TPs (incubation day 15) were injected repeatedly into the HPLC system, running under conditions as described above. The radioactive fractions were collected separately, evaporated to dryness under a gentle stream of nitrogen gas, and resuspended in 200 μL of methanol for further analysis by gas chromatography−mass spectrometry (GC−MS) as described in the Supporting Information. LC−MS. LC analysis was performed on a Beta Basic−C18 column with a Finnigan Surveyor LC system. MS was performed on a Finnigan LCQ Advantage MAX ion trap mass spectrometer (Thermo, USA; for details, see the Supporting Information). Determination of Radioactivity. Radioactivity was quantitatively determined on a LSC (LS6500, Beckman Coulter, USA) with external standards. For determination of the radioactivity of 14CO2 trapped in NaOH, 1 mL of this solution was mixed with 15 mL of scintillation cocktail (Lumasafe Plus, Lumac LSC, Groningen, The Netherlands). For the radioactivity in organic extracts and the bound radioactivity in the sludge, 1 mL of extract or sludge was mixed with 15 mL of

3. RESULTS AND DISCUSSION 3.1. Fate of TBBPA in NAS. During the 31-day incubation, TBBPA was transformed and mineralized in NAS in the presence or absence of the inhibitor ATU (50 mg/L). Figure 1 shows the amounts of 14CO2 and the extractable and bound

Figure 1. Radioactivity recovered from organic extracts, bound residues (left y-axis), and 14CO2 (right y-axis) during the incubation of 14C-TBBPA in nitrifying activated sludge (NAS) without (a) and with (b) the addition of 50 mg ATU/L and in sterilized sludge (c). Values are the means and standard deviations of three individual experiments. 4285

DOI: 10.1021/es5059007 Environ. Sci. Technol. 2015, 49, 4283−4292

Article

Environmental Science & Technology radioactivities from 14C-TBBPA in the sludges during the incubation. Ammonia-oxidizing activity in NAS without the addition of ATU was always >30 mg N/g SS/h upon the addition of fresh NH4+ and mineralization occurred without a lag phase, accounting for 17.0 ± 0.7% of the initial 14C-TBBPA at the end of the incubation (Figure 1a). Mineralization was accompanied by a decrease in extractable radioactivity and the increasing formation of bound residues in the sludge (Figure 1a). At the end of the incubation, the amount of extractable radioactivity decreased to 27.2 ± 0.9% of the initial radioactivity, while the amount of bound radioactivity increased to 55.8 ± 0.4% (Figure 1a). In the sludge with ATU addition, ammonia-oxidizing activity was 7.0 than at pH 6.5 for EE2.41 The amenability of TBBPA to nitration by nitrite is probably due to the easier loss from the benzene ring of a bromine rather than a hydrogen or carbonic substituents. Although radical reactions are responsible for the abiotic nitration of halogen-free phenols, such as paracetamol, BPA, and o-phenylphenol,42,44 nucleophilic substitution occurs in the abiotic nitro debromination of TBBPA. 3.4. Role of AOMs in Transformation of TBBPA in NAS. Nitrifying activity in the sludge may have been carried out by autotrophs and/or heterotrophs. However, in contrast to autotrophic nitrifiers, heterotrophic nitrifiers are generally insensitive to ATU.60 Since the addition of 50 mg of ATU/L to NAS immediately stopped ammonia-oxidizing activity (Figure 3b), the role played by heterotrophic nitrifiers in total ammonia oxidation in the sludge must have been negligible. This result is consistent with previous studies in which AOB were the major contributors to ammonia oxidation in both a highly aerated activated sludge bioreactor61 and a laboratory-scale nitrogen-removing reactor.62 The recovery of



ASSOCIATED CONTENT

S Supporting Information *

Methods of analyses, identification of the TPs, and the mass spectra of the trimethylsilylated derivatives of the identified TPs are provided. This material is available free of charge via the Internet at http://pubs.acs.org/. 4289

DOI: 10.1021/es5059007 Environ. Sci. Technol. 2015, 49, 4283−4292

Article

Environmental Science & Technology



(15) Brenner, A.; Mukmenev, I.; Abeliovich, A.; Kushmaro, A. Biodegradability of tetrabromobisphenol A and tribromophenol by activated sludge. Ecotoxicology 2006, 15, 399−402. (16) Nyholm, J. R.; Lundberg, C.; Andersson, P. L. Biodegradation kinetics of selected brominated flame retardants in aerobic and anaerobic soil. Environ. Pollut. 2010, 158, 2235−2240. (17) Ronen, Z.; Abeliovich, A. Anaerobic-aerobic process for microbial degradation of tetrabromobisphenol A. Appl. Environ. Microbiol. 2000, 66, 2372−2377. (18) Voordeckers, J. W.; Fennell, D. E.; Jones, K.; Häggblom, M. M. Anaerobic biotransformation of tetrabromobisphenol A, tetrachlorobisphenol A, and bisphenol A in estuarine sediments. Environ. Sci. Technol. 2002, 36, 696−701. (19) Arbeli, Z.; Ronen, Z.; Díaz-Báez, M. C. Reductive dehalogenation of tetrabromobisphenol-A by sediment from a contaminated ephemeral streambed and an enrichment culture. Chemosphere 2006, 64, 1472−1478. (20) Gerecke, A. C.; Giger, W.; Hartmann, P. C.; Heeb, N. V.; Kohler, H. P.; Schmid, P.; Zennegg, M.; Kohler, M. Anaerobic degradation of brominated flame retardants in sewage sludge. Chemosphere 2006, 64, 311−317. (21) Peng, F. Q.; Ying, G. G.; Yang, B.; Liu, Y. S.; Lai, H. J.; Zhou, G. J.; Chen, J.; Zhao, J. L. Biotransformation of the flame retardant tetrabromobisphenol-A (TBBPA) by freshwater microalgae. Environ. Toxicol. Chem. 2014, 33, 1705−1711. (22) Watanabe, I.; Kashimoto, T.; Tatsukawa, R. The flame retardant tetrabromobisphenol A and its metabolite found in river and marine sediments in Japan. Chemosphere 1983, 12, 1533−1539. (23) Sellström, U.; Jansson, B. Analysis of tetrabromobisphenol A in a product and environmental samples. Chemosphere 1995, 31, 3085− 3092. (24) George, K. W.; Häggblom, M. M. Microbial O-methylation of the flame retardant tetrabromobisphenol-A. Environ. Sci. Technol. 2008, 42, 5555−5561. (25) Morris, S.; Allchin, C. R.; Zegers, B. N.; Haftka, J. J. H.; Boon, J. P.; Belpaire, C.; Leonards, P. E. G.; Van Leeuwen, S. P. J.; De Boer, J. Distribution and fate of HBCD and TBBPA brominated flame retardants in north sea estuaries and aquatic food webs. Environ. Sci. Technol. 2004, 38, 5497−5504. (26) Ő berg, K.; Warman, K.; Ő berg, T. Distribution and levels of brominated flame retardants in sewage sludge. Chemosphere 2002, 48, 805−809. (27) Chu, S.; Haffner, G. D.; Letcher, R. J. Simultaneous determination of tetrabromobisphenol A, tetrachlorobisphenol A, bisphenol A and other halogenated analogues in sediment and sludge by high performance liquid chromatography-electrospray tandem mass spectrometry. J. Chromatogr. A 2005, 1097, 25−32. (28) Hwang, I. K.; Kang, H. H.; Lee, I. S.; Oh, J. E. Assessment of characteristic distribution of PCDD/Fs and BFRs in sludge generated at municipal and industrial wastewater treatment plants. Chemosphere 2012, 88, 888−894. (29) Gorga, M.; Martinez, E.; Ginebreda, A.; Eljarrat, E.; Barceló, D. Determination of PBDEs, HBB, PBEB, DBDPE, HBCD, TBBPA and related compounds in sewage sludge from Catalonia (Spain). Sci. Total Environ. 2013, 444, 51−59. (30) Feng, A. H.; Chen, S. J.; Chen, M. Y.; He, M. J.; Luo, X. J.; Mai, B. X. Hexabromocyclododecane (HBCD) and tetrabromobisphenol A (TBBPA) in riverine and estuarine sediments of the Pearl River Delta in southern China, with emphasis on spatial variability in diastereoisomer- and enantiomer-specific distribution of HBCD. Mar. Pollut. Bull. 2012, 64, 919−925. (31) Song, S. J.; Song, M. Y.; Zeng, L. Z.; Wang, L. Z.; Liu, R. Z.; Ruan, T.; Jiang, G. B. Occurrence and profiles of bisphenol analogues in municipal sewage sludge in China. Environ. Pollut. 2014, 186, 14− 19. (32) Hansen, A. B.; Lassen, P. Screening of phenolic substances in the Nordic environments; Nordic Council of Ministers: Copenhagen, 2008. (33) Kuramochi, H.; Kawamoto, K.; Miyazaki, K.; Nagahama, K.; Maeda, K.; Li, X. W.; Shibata, E.; Nakamura, T.; Sakai, S.

AUTHOR INFORMATION

Corresponding Author

*Tel: +86-25-8968 0581. E-mail: [email protected]. Notes

The authors declare no competing financial interest.



ACKNOWLEDGMENTS This work was supported by the National Natural Science Foundation of China (NSFC) (Grant Nos. 21237001 and 21177057), the Sino-Swiss Science and Technology Cooperation (SSSTC) (Grant No. IZLCZ2_138846), and the earmarked cooperation project of the State Key Laboratory of Pollution Control and Resource Reuse (Grant No. PCRRF12022).



REFERENCES

(1) de Wit, C. A. An overview of brominated flame retardants in the environment. Chemosphere 2002, 46, 583−624. (2) Law, R. J.; Allchin, C. R.; de Boer, J.; Covaci, A.; Herzke, D.; Lepom, P.; Morris, S.; Tronczynski, J.; de Wit, C. A. Levels and trends of brominated flame retardants in the European environment. Chemosphere 2006, 64, 187−208. (3) Covaci, A.; Voorspoels, S.; Abdallah, M. A.-E.; Geens, T.; Harrad, S.; Law, R. J. Analytical and environmental aspects of the flame retardant tetrabromobisphenol-A and its derivatives. J. Chromatogr. A 2009, 1216, 346−363. (4) Harrad, S.; Abdallah, M. A-E.; Rose, N. L.; Turner, S. D.; Davidson, T. A. Current-use brominated flame retardants in water, sediment, and fish from English lakes. Environ. Sci. Technol. 2009, 43, 9077−9083. (5) Luo, X. J.; Zhang, X. L.; Chen, S. J.; Mai, B. X. Free and bound polybrominated diphenyl ethers and tetrabromobisphenol A in freshwater sediments. Mar. Pollut. Bull. 2010, 60, 718−724. (6) Sánchez-Brunete, C.; Miquel, E.; Tadeo, J. L. Determination of tetrabromobisphenol-A, tetrachlorobisphenol-A and bisphenol-A in soil by ultrasonic assisted extraction and gas chromatography−mass spectrometry. J. Chromatogr. A 2009, 1216, 5497−5503. (7) Zhang, X. L.; Luo, X. J.; Chen, S. J.; Wu, J. P.; Mai, B. X. Spatial distribution and vertical profile of polybrominated diphenyl ethers, tetrabromobisphenol A, and decabromodiphenylethane in river sediment from an industrialized region of South China. Environ. Pollut. 2009, 157, 1917−1923. (8) Birnbaum, L. S.; Staskal, D. F. Brominated flame retardants: cause for concern? Environ. Health Perspect. 2004, 112, 9−17. (9) Fukuda, N.; Ito, Y.; Yamaguchi, M.; Mitumori, K.; Koizumi, M.; Hasegawa, R.; Kamata, E.; Ema, M. Unexpected nephrotoxicity induced by tetrabromobisphenol A in newborn rats. Toxicol. Lett. 2004, 150, 145−155. (10) Tada, Y.; Fujitani, T.; Ogata, A.; Kamimura, H. Flame retardant tetrabromobisphenol A induced hepatic changes in ICR male mice. Environ. Toxicol. Pharmacol. 2007, 23, 174−178. (11) Hakk, H.; Letcher, R. J. Metabolism in the toxicokinetics and fate of brominated flame retardants−a review. Environ. Int. 2003, 29, 801−828. (12) Liu, J.; Wang, Y. F.; Jiang, B. Q.; Wang, L. H.; Chen, J. Q.; Guo, H. Y.; Ji, R. Degradation, metabolism, and bound-residue formation and release of tetrabromobisphenol A in soil during sequential anoxicoxic incubation. Environ. Sci. Technol. 2013, 47, 8348−8354. (13) Li, F. J.; Wang, J. J.; Nastold, P.; Jiang, B. Q.; Sun, F. F.; Zenker, A.; Kolvenbach, B. A.; Ji, R.; Corvini, P. F. X. Fate and metabolism of tetrabromobisphenol A in soil slurries without and with the amendment with the alkylphenol degrading bacterium Sphingomonas sp. strain TTNP3. Environ. Pollut. 2014, 193, 181−188. (14) Ravit, B.; Ehrenfeld, J. G.; Häggblom, M. M. Salt marsh rhizosphere affects microbial biotransformation of the widespread halogenated contaminant tetrabromobisphenol-A (TBBPA). Soil Biol. Biochem. 2005, 37, 1049−1057. 4290

DOI: 10.1021/es5059007 Environ. Sci. Technol. 2015, 49, 4283−4292

Article

Environmental Science & Technology Determination of physicochemical properties of tetrabromobisphenol A. Environ. Toxicol. Chem. 2008, 27, 2413−2418. (34) An, T. C.; Zu, L.; Li, G. Y.; Wan, S. G.; Mai, B. X.; Wong, P. K. One-step process for debromination and aerobic mineralization of tetrabromobisphenol-A by a novel Ochrobactrum sp. T isolated from an e-waste recycling site. Bioresour. Technol. 2011, 102, 9148−9154. (35) Peng, X. X.; Zhang, Z. L.; Luo, W. S.; Jia, X. S. Biodegradation of tetrabromobisphenol A by a novel Comamonas sp. strain, JXS-2-02, isolated from anaerobic sludge. Bioresour. Technol. 2013, 128, 173− 179. (36) Joss, A.; Zabczynski, S.; Göbel, A.; Hoffmann, B.; Löffler, D.; McArdell, C. S.; Ternes, T. A.; Thomsen, A.; Siegrist, H. Biological degradation of pharmaceuticals in municipal wastewater treatment: Proposing a classification scheme. Wat. Res. 2006, 40, 1686−1696. (37) Sayavedra-Soto, L. A.; Gvakharia, B.; Bottomley, P. J.; Arp, D. J.; Dolan, M. E. Nitrification and degradation of halogenated hydrocarbon−a tenuous balance for ammonia-oxidizing bacteria. Appl. Microbiol. Biotechnol. 2010, 86, 435−444. (38) Vader, J. S.; van Ginkel, C. G.; Sperling, F. M. G. M.; de Jong, J.; de Boer, W.; de Graaf, J. S.; van der Most, M.; Stokman, P. G. W. Degradation of ethinyl estradiol by nitrifying activated sludge. Chemosphere 2000, 41, 1239−1243. (39) Shi, J. H.; Fujisawa, S.; Nakai, S.; Hosomi, M. Biodegradation of natural and synthetic estrogens by nitrifying activated sludge and ammonia-oxidizing bacterium Nitrosomonas europaea. Wat. Res. 2004, 38, 2323−2330. (40) Yi, T.; Harper, W. F., Jr. The link between nitrification and biotransformation of 17α-ethinylestradiol. Environ. Sci. Technol. 2007, 41, 4311−4316. (41) Gaulke, L. S.; Strand, S. E.; Kalhorn, T. F.; Stensel, H. D. 17αEthinylestradiol. transformation via abiotic nitration in the presence of ammonia oxidizing bacteria. Environ. Sci. Technol. 2008, 42, 7622− 7627. (42) Chiron, S.; Gomez, E.; Fenet, H. Nitration processes of acetaminophen in nitrifying activated sludge. Environ. Sci. Technol. 2010, 44, 284−289. (43) Skotnicka-Pitak, J.; Khunjar, W. O.; Love, N. G.; Aga, D. S. Characterization of metabolites formed during the biotransformation of 17α-ethinylestradiol by Nitrosomonas europaea in batch and continuous flow bioreactors. Environ. Sci. Technol. 2009, 43, 3549− 3555. (44) Jewell, K. S.; Wick, A.; Ternes, T. A. Comparisons between abiotic nitration and biotransformation reactions of phenolic micropollutants in activated sludge. Wat. Res. 2014, 48, 478−489. (45) Khunjar, W. O.; Mackintosh, S. A.; Skotnicka-Pitak, J.; Baik, S.; Aga, D. S.; Love, N. G. Elucidating the relative roles of ammonia oxidizing and heterotrophic bacteria during the biotransformation of 17α-ethinylestradiol and trimethoprim. Environ. Sci. Technol. 2011, 45, 3605−3612. (46) Potvin, C. M.; Long, Z. B.; Zhou, H. D. Removal of tetrabromobisphenol A by conventional activated sludge, submerged membrane and membrane aerated biofilm reactors. Chemosphere 2012, 89, 1183−1188. (47) Ren, Y. X.; Nakano, K.; Nomura, M.; Chiba, N.; Nishimura, O. Effects of bacterial activity on estrogen removal in nitrifying activated sludge. Wat. Res. 2007, 41, 3089−3096. (48) Feng, Y.; Colosi, L. M.; Gao, S. X.; Huang, Q. G.; Mao, L. Transformation and removal of tetrabromobisphenol A from water in the presence of natural organic matter via laccase-catalyzed reactions: reaction rates, products, and pathways. Environ. Sci. Technol. 2013, 47, 1001−1008. (49) Lin, K. D.; Liu, W. P.; Gan, J. Reaction of tetrabromobisphenol A (TBBPA) with manganese dioxide: kinetics, products, and pathways. Environ. Sci. Technol. 2009, 43, 4480−4486. (50) Li, C. L.; Ji, R.; Vinken, R.; Hommes, G.; Bertmer, M.; Schäffer, A.; Corvini, P. F. X. Role of dissolved humic acids in the biodegradation of a single isomer of nonylphenol by Sphingomonas sp. Chemosphere 2007, 68, 2172−2180.

(51) Li, C. L.; Zhang, B.; Ertunc, T.; Schäffer, A.; Ji, R. Birnessiteinduced binding of phenolic monomers to soil humic substances and nature of the bound residues. Environ. Sci. Technol. 2012, 46, 8843− 8850. (52) Riefer, P.; Klausmeyer, T.; Adams, A.; Schmidt, B.; Schäffer, A.; Schwarzbauer, J. Incorporation mechanisms of a branched nonylphenol isomer in soil-derived organo-clay complexes during a 180day experiment. Environ. Sci. Technol. 2013, 47, 7155−7162. (53) Corvini, P. F. X.; Hollender, J.; Ji, R.; Schumacher, S.; Prell, J.; Hommes, G.; Priefer, U.; Vinken, R.; Schäffer, A. The degradation of α-quaternary nonylphenol isomers by Sphingomonas sp. strain TTNP3 involves a type II ipso-substitution mechanism. Appl. Microbiol. Biotechnol. 2006, 70, 114−122. (54) Gabriel, F. L. P.; Heidlberger, A.; Rentsch, D.; Giger, W.; Guenther, K.; Kohler, H. P. E. A novel metabolic pathway for degradation of 4-nonylphenol environmental contaminants by Sphingomonas xenophaga Bayram: ipso-hydroxylation and intramolecular rearrangement. J. Biol. Chem. 2005, 280, 15526−15533. (55) Sun, Q.; Li, Y.; Chou, P.-H.; Peng, P. Y.; Yu, C. P. Transformation of bisphenol A and alkylphenols by ammoniaoxidizing bacteria through nitration. Environ. Sci. Technol. 2012, 46, 4442−4448. (56) Telscher, M. J. H.; Schuller, U.; Schmidt, B.; Schäfer, A. Occurrence of a nitro metabolite of a defined nonylphenol isomer in soil/sewage sludge mixtures. Environ. Sci. Technol. 2005, 39, 7896− 7900. (57) Zhang, H.; Spiteller, M.; Guenther, K.; Boehmler, G.; Zuehlke, S. Degradation of a chiral nonylphenol isomer in two agricultural soils. Environ. Pollut. 2009, 157, 1904−1910. (58) De Weert, J.; Viñas, M.; Grotenhuis, T.; Rijnaarts, H.; Langenhoff, A. Aerobic nonylphenol degradation and nitro-nonylphenol formation by microbial cultures from sediments. Appl. Microbiol. Biotechnol. 2010, 86, 761−771. (59) Wick, A.; Wagner, M.; Ternes, T. A. Elucidation of the transformation pathways of the opium alkaloid codeine in biological wastewater treatment. Environ. Sci. Technol. 2011, 45, 3374−3385. (60) Wagner, M.; Rath, G.; Amann, R.; Koops, H.-P.; Schleifer, K.-H. In situ identification of ammonia-oxidizing bacteria. System. Appl. Microbiol. 1995, 18, 251−264. (61) Wells, G. F.; Park, H.-D.; Yeung, C.-H.; Eggleston, B.; Francis, C. A.; Criddle, C. S. Ammonia-oxidizing communities in a highly aerated full-scale activated sludge bioreactor: betaproteobacterial dynamics and low relative abundance of Crenarchaea. Environ. Microbiol. 2009, 11, 2310−2328. (62) Jin, T.; Zhang, T.; Yan, Q. M. Characterization and quantification of ammonia-oxidizing archaea (AOA) and bacteria (AOB) in a nitrogen-removing reactor using T-RFLP and qPCR. Appl. Microbiol. Biotechnol. 2010, 87, 1167−1176. (63) Keener, W. K.; Arp, D. J. Transformations of aromatic compounds by Nitrosomonas europaea. Appl. Environ. Microbiol. 1994, 60, 1914−1920. (64) Hooper, A. B.; Vannelli, T.; Bergmann, D. J.; Arciero, D. M. Enzymology of the oxidation of ammonia to nitrite by bacteria. Antonie van Leeuwenhoek 1997, 71, 59−67. (65) Nakamura, S.; Tezuka, Y.; Ushiyama, A.; Kawashima, C.; Kitagawara, Y.; Takahashi, K.; Ohta, S.; Mashino, T. Ipso substitution of bisphenol A catalyzed by microsomal cytochrome P450 and enhancement of estrogenic activity. Toxicol. Lett. 2011, 203, 92−95. (66) Spivack, J.; Leib, T. K.; Lobos, J. H. Novel pathway for bacterial metabolism of bisphenol A. Rearrangements and stilbene cleavage in bisphenol A metabolism. J. Biol. Chem. 1994, 269, 7323−7329. (67) Sasaki, M.; Akahira, A.; Oshiman, K.; Tsuchido, T.; Matsumura, Y. Purification of cytochrome P450 and ferredoxin, involved in bisphenol A degradation, from Sphingomonas sp. strain AO1. Appl. Environ. Microbiol. 2005, 71, 8024−8030. (68) Eichenbaum, G.; Johnson, M.; Kirkland, D.; O’Neill, P.; Stellar, S.; Bielawne, J.; DeWire, R.; Areia, D.; Bryant, S.; Weiner, S.; DesaiKrieger, D.; Guzzie-Peck, P.; Evans, D. C.; Tonelli, A. Assessment of the genotoxic and carcinogenic risks of p-nitrophenol when it is 4291

DOI: 10.1021/es5059007 Environ. Sci. Technol. 2015, 49, 4283−4292

Article

Environmental Science & Technology present as an impurity in a drug product. Requl. Toxicol. Pharmacol. 2009, 55, 33−42. (69) Mulder, J. W.; van Loosdrecht, M. C. M.; Hellinga, C.; van Kempen, R. Full-scale application of the SHARON process for treatment of rejection water of digested sludge dewatering. Wat. Sci. Technol. 2001, 43, 127−134. (70) Ruiz, G.; Jeison, D.; Rubilar, O.; Ciudad, G.; Chamy, R. Nitrification-denitrification via nitrite accumulation for nitrogen removal from wastewaters. Bioresour. Technol. 2006, 97, 330−335.

4292

DOI: 10.1021/es5059007 Environ. Sci. Technol. 2015, 49, 4283−4292